Cryptic splice activation but not exon skipping is observed in minigene assays of dystrophin c.9361+1G>A mutation identified by NGS

Journal of Human Genetics

Volumn 62, Issue 5, 2017, Pages 531-537

  Niba, Emma Tabe Eko ^a   Nishida, Atsushi ^a   Tran, Van Khanh ^b   Vu, Dung Chi ^c   Matsumoto, Masaaki ^d   Awano, Hiroyuki ^d   Lee, Tomoko ^e   Takeshima, Yasuhiro ^e   Nishio, Hisahide ^d   Matsuo, Masafumi ^a  

^a KOBE GAKUIN UNIVERSITY   (Japan)

^b HANOI MEDICAL UNIVERSITY   (Viet Nam)

^c NATIONAL HOSPITAL OF PEDIATRICS   (Viet Nam)

^d KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN;

ARTICLE; BECKER MUSCULAR DYSTROPHY; CASE REPORT; CHILD; DYSTROPHINOPATHY; EXON SKIPPING; FRAMESHIFT MUTATION; HUMAN; INTRON RETENTION; MALE; MUSCLE WEAKNESS; NEXT GENERATION SEQUENCING; OPEN READING FRAME; RNA SPLICING; SANGER SEQUENCING; SCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; EXON; GENETICS; HIGH THROUGHPUT SEQUENCING; INTRON; MUTATION; NUCLEOTIDE SEQUENCE; PRESCHOOL CHILD; PROCEDURES; RNA SPLICE SITE;

BASE SEQUENCE; CHILD; CHILD, PRESCHOOL; DYSTROPHIN; EXONS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INTRONS; MALE; MUTATION; RNA SPLICE SITES; RNA SPLICING;

EID: 85018748923     PISSN: 14345161     EISSN: 1435232X     Source Type: Journal    
DOI: 10.1038/jhg.2016.162     Document Type: Article

References (43)

1. Aartsma-Rus, A., Van Deutekom, J. C., Fokkema, I. F., Van Ommen, G. J., & Den Dunnen, J. T. Entries in the Leiden Duchenne muscular dystrophy mutation database: an overview of mutation types and paradoxical cases that confirm the readingframe rule. Muscle Nerve 34, 135-144 (2006
2. Takeshima, Y., Yagi, M., Okizuka, Y., Awano, H., Zhang, Z., Yamauchi, Y., et al. Mutation spectrum of the dystrophin gene in 442 Duchenne/Becker muscular dystrophy cases from one Japanese referral center. J. Hum. Genet. 55, 379-388 (2010
3. Rehm, H. L. Disease-Targeted sequencing: a cornerstone in the clinic. Nat. Rev. Genet. 14, 295-300 (2013
4. Sikkema-Raddatz, B., Johansson, L. F., de Boer, E. N., Almomani, R., Boven, L. G., van den Berg, M. P., et al. Targeted next-generation sequencing can replace Sanger sequencing in clinical diagnostics. Hum. Mutat. 34, 1035-1042 (2013
5. Valencia, C. A., Ankala, A., Rhodenizer, D., Bhide, S., Littlejohn, M. R., Keong, L. M., et al. Comprehensive mutation analysis for congenital muscular dystrophy: a clinical PCR-based enrichment and next-generation sequencing panel. PLoS ONE 8, e53083 (2013
6. Niba, E. T., Tran, V. K., Tuan-Pham, L. A., Vu, D. C., Nguyen, N. K., Ta, V. T., et al. Validation of ambiguous MLPA results by targeted next-generation sequencing discloses a nonsense mutation in the DMD gene. Clin. Chim. Acta 436, 155-159 (2014
7. Roucher Boulez, F., Menassa, R., Streichenberger, N., Manel, V., Mallet-Motak, D., Morel, Y., et al. A splicing mutation in the DMD gene detected by next-generation sequencing and confirmed by mRNA and protein analysis. Clin. Chim. Acta 448, 146-149 (2015
8. Taniguchi-Ikeda, M., Takeshima, Y., Lee, T., Nishiyama, M., Awano, H., Yagi, M., et al. Next-generation sequencing discloses a nonsense mutation in the dystrophin gene from long preserved dried umbilical cord and low-level somatic mosaicism in the proband mother. J. Hum. Genet. 61, 351-355 (2016
9. Okubo, M., Minami, N., Goto, K., Goto, Y., Noguchi, S., Mitsuhashi, S., et al. Genetic diagnosis of Duchenne/Becker muscular dystrophy using next-generation sequencing: validation analysis of DMD mutations. J. Hum. Genet. 61, 483-489 (2016
10. Monaco, A. P., Bertelson, C. J., Liechti-Gallati, S., Moser, H., & Kunkel, L. M. An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics 2, 90-95 (1988
11. Ahn, A. H., & Kunkel, L. M. The structural and functional diversity of dystrophin. Nat. Genet. 3, 283-291 (1993
12. Zhang, Z., Habara, Y., Nishiyama, A., Oyazato, Y., Yagi, M., Takeshima, Y., et al. Identification of seven novel cryptic exons embedded in the dystrophin gene and characterization of 14 cryptic dystrophin exons. J. Hum. Genet. 52, 607-617 (2007
13. Nishida, A., Minegishi, M., Takeuchi, A., Awano, H., Niba, E. T., & Matsuo, M. Neuronal SH-SY5Y cells use the C-dystrophin promoter coupled with exon 78 skipping and display multiple patterns of alternative splicing including two intronic insertion events. Hum. Genet. 134, 993-1001 (2015
14. Gazzoli, I., Pulyakhina, I., Verwey, N. E., Ariyurek, Y., Laros, J. F., Hoen, P. A., et al. Non-sequential and multi-step splicing of the dystrophin transcript. RNA Biol. 13, 290-305 (2016
15. Flanigan, K. M., Dunn, D. M., von Niederhausern, A., Soltanzadeh, P., Howard, M. T., Sampson, J. B., et al. Nonsense mutation-Associated Becker muscular dystrophy: interplay between exon definition and splicing regulatory elements within the DMD gene. Hum. Mutat. 32, 299-308 (2011
16. Tran, V. K., Takeshima, Y., Zhang, Z., Yagi, M., Nishiyama, A., Habara, Y., et al. Splicing analysis disclosed a determinant single nucleotide for exon skipping caused by a novel intra-exonic four-nucleotide deletion in the dystrophin gene. J. Med. Genet. 43, 924-930 (2006
17. Magri, F., Del Bo, R., D'Angelo, M. G., Govoni, A., Ghezzi, S., Gandossini, S., et al. Clinical and molecular characterization of a cohort of patients with novel nucleotide alterations of the Dystrophin gene detected by direct sequencing. BMC Med. Genet. 12, 37 (2011
18. Wimmer, K., Roca, X., Beiglböck, H., Callens, T., Etzler, J., Rao, A., et al. Extensive in silico analysis of NF1 splicing defects uncovers determinants for splicing outcome upon 5' splice-site disruption. Hum. Mutat. 28, 599-612 (2007
19. Baralle, D., & Baralle, M. Splicing in action: assessing disease causing sequence changes. J. Med. Genet. 42, 737-748 (2005
20. Krawczak, M., Thomas, N. S. T., Hundrieser, B., Mort, M., Wittig, M., Hampe, J., et al. Single base-pair substitutions in exon-intron junctions of human genes: nature, distribution, and consequences for mRNA splicing. Hum. Mutat. 28, 150-158 (2007
21. ElSharawy, A., Hundrieser, B., Brosch, M., Wittig, M., Huse, K., Platzer, M., et al. Systematic evaluation of the effect of common SNPs on pre-mRNA splicing. Hum. Mutat. 30, 625-632 (2009
22. Takeshima, Y., Yagi, M., Wada, H., Ishibashi, K., Nishiyama, A., Kakumoto, M., et al. Intravenous infusion of an antisense oligonucleotide results in exon skipping in muscle dystrophin mRNA of Duchenne muscular dystrophy. Pediatr. Res. 59, 690-694 (2006
23. Lewandowska, M. A. The missing puzzle piece: splicing mutations. Int. J. Clin. Exp. Pathol. 6, 2675-2682 (2013
24. Gaildrat, P., Killian, A., Martins, A., Tournier, I., Frebourg, T., & Tosi, M. Use of splicing reporter minigene assay to evaluate the effect on splicing of unclassified genetic variants. Methods Mol. Biol. 653, 249-257 (2010
25. Takeshima, Y., Nishio, H., Sakamoto, H., Nakamura, H., & Matsuo, M. Modulation of in vitro splicing of the upstream intron by modifying an intra-exon sequence which is deleted from the dystrophin gene in dystrophin Kobe. J. Clin. Invest. 95, 515-520 (1995
26. Wang, Z., Lin, Y., Qiu, L., Zheng, D., Yan, A., Zeng, J., et al. Hybrid minigene splicing assay verified the pathogenicity of a novel splice site variant in the dystrophin gene of a Chinese patient with typical Duchenne muscular dystrophy phenotype. Clin. Chem. Lab. Med. 54, 1435-1440 (2016
27. Habara, Y., Takeshima, Y., Awano, H., Okizuka, Y., Zhang, Z., Saiki, K., et al. In vitro splicing analysis showed that availability of a cryptic splice site is not a determinant for alternative splicing patterns caused by +1G-4A mutations in introns of the dystrophin gene. J. Med. Genet. 46, 542-547 (2009
28. Habara, Y., Doshita, M., Hirozawa, S., Yokono, Y., Yagi, M., Takeshima, Y., et al. A strong exonic splicing enhancer in dystrophin exon 19 achieve proper splicing without an upstream polypyrimidine tract. J. Biochem. 143, 303-310 (2008
29. Nishida, A., Kataoka, N., Takeshima, Y., Yagi, M., Awano, H., Ota, M., et al. Chemical treatment enhances skipping of a mutated exon in the dystrophin gene. Nat. Commun. 2, 308 (2011
30. Desmet, F. O., Hamroun, D., Lalande, M., Collod-Beroud, G., Claustres, M., & Beroud, C. Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res. 37, e67 (2009
31. Yeo, G., & Burge, C. B. Maximum entrophy modeling of short sequence motifs with applications to RNA splicing signals. J. Comput. Biol. 11, 377-394 (2003
32. Sironi, M., Menozzi, G., Riva, L., Cagliani, R., Comi, G. P., Bresolin, N., et al. Silencer elements as possible inhibitors of pseudoexon splicing. Nucleic Acids Res. 32, 1783-1791 (2004
33. Wang, Y., Ma, M., Xiao, X., & Wang, Z. Intronic splicing enhancers, cognate splicing factors and context-dependent regulation rules. Nat. Struct. Mol. Biol. 19, 1044-1052 (2012
34. Flanigan, K. M., Dunn, D. M., von Niederhausern, A., Soltanzadeh, P., Gappmaier, E., Howard, M. T., et al. Mutational spectrum of DMD mutations in dystrophinopathy patients: application of modern diagnostic techniques to a large cohort. Hum. Mutat. 30, 1657-1666 (2009
35. Seo, S., Takayama, K., Uno, K., Ohi, K., Hashimoto, R., Nishizawa, D., et al. Functional analysis of deep intronic SNP rs13438494 in intron 24 of PCLO gene. PLoS ONE 8, e76960 (2013
36. Kashima, T., Rao, N., & Manley, J. L. An intronic element contributes to splicing repression in spinal muscular atrophy. Proc. Natl Acad. Sci. USA 104, 3426-3431 (2007
37. Thi Tran, H. T., Takeshima, Y., Surono, A., Yagi, M., Wada, H., & Matsuo, M. A G-To-A transition at the fifth position of intron 32 of the dystrophin gene inactivates a splice donor site both in vivo and in vitro. Mol. Genet. Metab. 85, 213-219 (2005
38. Deburgrave, N., Daoud, F., Llense, S., Barbot, J. C., Recan, D., Peccate, C., et al. Protein- And mRNA-based phenotype-genotype correlations in DMD/BMD with point mutations and molecular basis for BMD with nonsense and frameshift mutations in the DMD gene. Hum. Mutat. 28, 183-195 (2007
39. Aartsma-Rus, A., Fokkema, I., Verschuuren, J., Ginjaar, I., van Deutekom, J., van Ommen, G. J., et al. Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Hum. Mutat. 30, 293-299 (2009
40. Matsuo, M., Takeshima, Y., & Nishio, H. Contributions of Japanese patients to development of antisense therapy for DMD. Brain Dev. 38, 4-9 (2016
41. Mendell, J. R., Goemans, N., Lowes, L. P., Alfano, L. N., Berry, K., Shao, J., et al. Longitudinal effect of eteplirsen versus historical control on ambulation in Duchenne muscular dystrophy. Ann. Neurol. 79, 257-271 (2016
42. Matsuo, M., Masumura, T., Nishio, H., Nakajima, T., Kitoh, Y., Takumi, T., et al. Exon skipping during splicing of dystrophin mRNA precursor due to an intraexon deletion in the dystrophin gene of Duchenne muscular dystrophy Kobe. J. Clin. Invest. 87, 2127-2131 (1991
43. Roest, P. A. M., Bout, M., van der Tuijn, A. C., Ginjaar, I. B., Bakker, E., Hogervorst, F. B. L., et al. Splicing mutations in DMD/BMD detected by RT-PCR/PTT: detection of a 19AA insertion in the cysteine rich domain of dystrophin compatible with BMD. J. Med. Genet. 33, 935-9396 (1996